Plasmodium falciparum Expressing Domain Cassette 5 Type PfEMP1 (DC5-PfEMP1) Bind PECAM1

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Berger, Sanne S ^a   Turner, Louise ^a   Wang, Christian W ^a   Petersen, Jens E V ^a   Kraft, Maria ^a   Lusingu, John P A ^b   Mmbando, Bruno ^b   Marquard, Andrea M ^a   Bengtsson, Dominique B A C ^a   Hviid, Lars ^a   Nielsen, Morten A ^a   Theander, Thor G ^a   Lavstsen, Thomas ^a  

^a Rigshospitalet   (Denmark)

^b NATIONAL INSTITUTE OF MEDICAL RESEARCH   (Tanzania)

Author keywords

[No Author keywords available]

Indexed keywords

CD31 ANTIGEN; DOMAIN CASSETTE 5 PLASMODIUM FALCIPARUM ERYTHROCYTE MEMBRANE PROTEIN 1 ANTIBODY; ERYTHROCYTE MEMBRANE PROTEIN 1; HEMOGLOBIN; PARASITE ANTIBODY; UNCLASSIFIED DRUG;

ADOLESCENT; ADULT; ANEMIA; ANTIBODY BLOOD LEVEL; ANTIBODY SPECIFICITY; ARTICLE; BONE MARROW CELL; CELL ADHESION; CELL SURFACE; CHILD; CONTROLLED STUDY; CROSS REACTION; ENDOTHELIUM CELL; FEVER; GENE CASSETTE; GENE SEQUENCE; GENETIC DIFFERENCE; GENETIC VARIABILITY; GENOME; HEMOGLOBIN BLOOD LEVEL; HUMAN; HUMAN CELL; INFANT; MAJOR CLINICAL STUDY; MALARIA; NONHUMAN; PHENOTYPE; PLASMODIUM FALCIPARUM; PRESCHOOL CHILD; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RAT; SCHOOL CHILD; SEQUENCE ANALYSIS;

ANTIBODIES, PROTOZOAN; ANTIGENS, CD31; ANTIGENS, PROTOZOAN; BONE MARROW CELLS; CLUSTER ANALYSIS; CONSERVED SEQUENCE; ENDOTHELIAL CELLS; ERYTHROCYTES; GENE EXPRESSION REGULATION; HUMANS; IMMUNOGLOBULIN G; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTOZOAN PROTEINS; TRANSCRIPTOME;

PLASMODIUM FALCIPARUM;

EID: 84879961302     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0069117     Document Type: Article

References (74)

1. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, et al. (2012) Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379: 413-431. doi:10.1016/S0140-6736(12)60034-8. PubMed: 22305225.
2. World Health Organization (2011) World malaria Report 2011, Geneva Switzerland.
3. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, et al. (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. doi:10.1016/0092-8674(95)90054-3. PubMed: 7541722.
4. 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. doi:10.1016/0092-8674(95)90056-X. PubMed: 7606775.
5. Su XZ, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, et al. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell 82: 89-100. doi:10.1016/0092-8674(95)90055-1. PubMed: 7606788.
6. Fried M, Duffy PE, (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science 272: 1502-1504. doi:10.1126/science.272.5267.1502. PubMed: 8633247.
7. 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. doi:10.1038/nm1297-1405. PubMed: 9396614.
8. 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. doi:10.1038/341057a0. PubMed: 2475784.
9. 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. doi:10.1172/JCI114234. PubMed: 2474574.
10. Clausen TM, Christoffersen S, Dahlbäck M, Langkilde AE, Jensen KE, et al. (2012) Structural and functional insight into how the Plasmodium falciparum VAR2CSA protein mediates binding to chondroitin sulfate A in placental malaria. J Biol Chem 287: 23332-23345. doi:10.1074/jbc.M112.348839. PubMed: 22570492.
11. Rowe JA, Claessens A, Corrigan RA, Arman M, (2009) Adhesion of Plasmodium falciparum-infected erythrocytes to human cells: molecular mechanisms and therapeutic implications. Expert Rev Mol Med 11: e16. doi:10.1017/S1462399409001082. PubMed: 19467172.
12. Hviid L, (2010) The role of Plasmodium falciparum variant surface antigens in protective immunity and vaccine development. Hum Vaccin 6: 84-89. doi:10.4161/hv.6.1.9602. PubMed: 19823032.
13. Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C, (1999) Immunity to non-cerebral severe malaria is acquired after one or two infections. Nat Med 5: 340-343. doi:10.1038/6560. PubMed: 10086393.
14. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, et al. (1998) Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat Med 4: 358-360. doi:10.1038/nm0398-358. PubMed: 9500614.
15. Bull PC, Lowe BS, Kortok M, Marsh K, (1999) Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect Immun 67: 733-739. PubMed: 9916084.
16. Bull PC, Kortok M, Kai O, Ndungu F, Ross A, et al. (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. doi:10.1086/315652. PubMed: 10882604.
17. Bull PC, Marsh K, (2002) The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria. Trends Microbiol 10: 55-58. doi:10.1016/S0966-842X(01)02278-8. PubMed: 11827798.
18. Bull PC, Berriman M, Kyes S, Quail MA, Hall N, et al. (2005) Plasmodium falciparum variant surface antigen expression patterns during malaria. PLOS Pathog 1: e26. doi:10.1371/journal.ppat.0010026. PubMed: 16304608.
19. Cham GK, Turner L, Lusingu J, Vestergaard L, Mmbando BP, et al. (2009) Sequential, ordered acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 domains. J Immunol 183: 3356-3363. doi:10.4049/jimmunol.0901331. PubMed: 19675168.
20. 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. doi:10.1084/jem.20040274. PubMed: 15123742.
21. Nielsen MA, Staalsoe T, Kurtzhals JA, Goka BQ, Dodoo D, et al. (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. PubMed: 11907103.
22. Bull PC, Buckee CO, Kyes S, Kortok MM, Thathy V, et al. (2008) Plasmodium falciparum antigenic variation. Mapping mosaic var gene sequences onto a network of shared, highly polymorphic sequence blocks. Mol Microbiol 68: 1519-1534. doi:10.1111/j.1365-2958.2008.06248.x. PubMed: 18433451.
23. Cham GK, Turner L, Kurtis JD, Mutabingwa T, Fried M, et al. (2010) Hierarchical, domain type-specific acquisition of antibodies to Plasmodium falciparum erythrocyte membrane protein 1 in Tanzanian children. Infect Immun 78: 4653-4659. doi:10.1128/IAI.00593-10. PubMed: 20823214.
24. Kalmbach Y, Rottmann M, Kombila M, Kremsner PG, Beck HP, et al. (2010) Differential var gene expression in children with malaria and antidromic effects on host gene expression. J Infect Dis 202: 313-317. doi:10.1086/653586. PubMed: 20540611.
25. Kyriacou HM, Stone GN, Challis RJ, Raza A, Lyke KE, et al. (2006) Differential var gene transcription in Plasmodium falciparum isolates from patients with cerebral malaria compared to hyperparasitaemia. Mol Biochem Parasitol 150: 211-218. doi:10.1016/j.molbiopara.2006.08.005. PubMed: 16996149.
26. Rottmann M, Lavstsen T, Mugasa JP, Kaestli M, Jensen AT, et al. (2006) Differential expression of var gene groups is associated with morbidity caused by Plasmodium falciparum infection in Tanzanian children. Infect Immun 74: 3904-3911. doi:10.1128/IAI.02073-05. PubMed: 16790763.
27. Warimwe GM, Keane TM, Fegan G, Musyoki JN, Newton CR, et al. (2009) Plasmodium falciparum var gene expression is modified by host immunity. Proc Natl Acad Sci U S A 106: 21801-21806. doi:10.1073/pnas.0907590106. PubMed: 20018734.
28. 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. doi:10.1186/1475-2875-2-27. PubMed: 14565852.
29. Rask TS, Hansen DA, Theander TG, Gorm PA, Lavstsen T, (2010) Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes--divide and conquer. PLOS Comput Biol 6: e1000933. PubMed: 20862303.
30. 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. doi:10.1046/j.1365-2958.2003.03570.x. PubMed: 12823820.
31. Salanti A, Dahlbäck 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. doi:10.1084/jem.20041579. PubMed: 15520249.
32. Magistrado P, Salanti A, Tuikue Ndam NG, Mwakalinga SB, Resende M, et al. (2008) VAR2CSA expression on the surface of placenta-derived Plasmodium falciparum-infected erythrocytes. J Infect Dis 198: 1071-1074. doi:10.1086/591502. PubMed: 18700835.
33. Bian Z, Wang G, (2000) Antigenic variation and cytoadherence of PfEMP1 of Plasmodium falciparum-infected erythrocyte from malaria patients. Chin Med J (Engl) 113: 981-984. PubMed: 11776131.
34. Kirchgatter K, Portillo HA, (2002) Association of severe noncerebral Plasmodium falciparum malaria in Brazil with expressed PfEMP1 DBL1 alpha sequences lacking cysteine residues. Mol Med 8: 16-23. PubMed: 11984002.
35. Falk N, Kaestli M, Qi W, Ott M, Baea K, et al. (2009) Analysis of Plasmodium falciparum var genes expressed in children from Papua New Guinea. J Infect Dis 200: 347-356. doi:10.1086/600071. PubMed: 19552523.
36. Kaestli M, Cockburn IA, Cortés A, Baea K, Rowe JA, et al. (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. doi:10.1086/503776. PubMed: 16652286.
37. Avril M, Tripathi AK, Brazier AJ, Andisi C, Janes JH, et al. (2012) A restricted subset of var genes mediates adherence of Plasmodium falciparum-infected erythrocytes to brain endothelial cells. Proc Natl Acad Sci U S A 109: E1782-E1790. doi:10.1073/pnas.1120534109. PubMed: 22619321.
38. Claessens A, Adams Y, Ghumra A, Lindergard G, Buchan CC, et al. (2012) A subset of group A-like var genes encodes the malaria parasite ligands for binding to human brain endothelial cells. Proc Natl Acad Sci U S A 109: E1772-E1781. doi:10.1073/pnas.1120992109. PubMed: 22619330.
39. 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. doi:10.1186/1475-2875-4-21. PubMed: 15857512.
40. 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. doi:10.1128/IAI.00951-06. PubMed: 17283085.
41. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797. doi:10.1093/nar/gkh340. PubMed: 15034147.
42. Hall TA, (1999) Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41: 95-98.
43. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599. doi:10.1093/molbev/msm092. PubMed: 17488738.
44. Crooks GE, Hon G, Chandonia JM, Brenner SE, (2004) WebLogo: a sequence logo generator. Genome Res 14: 1188-1190. doi:10.1101/gr.849004. PubMed: 15173120.
45. Cranmer SL, Magowan C, Liang J, Coppel RL, Cooke BM, (1997) An alternative to serum for cultivation of Plasmodium falciparum in vitro. Trans R Soc Trop Med Hyg 91: 363-365. doi:10.1016/S0035-9203(97)90110-3. PubMed: 9231219.
46. Schweitzer KM, Vicart P, Delouis C, Paulin D, Dräger AM, et al. (1997) Characterization of a newly established human bone marrow endothelial cell line: distinct adhesive properties for hematopoietic progenitors compared with human umbilical vein endothelial cells. Lab Invest 76: 25-36. PubMed: 9010447.
47. 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. doi:10.1111/j.1365-3024.2003.00652.x. PubMed: 14651589.
48. Moll K, Ljungström I, Perlmann H, Scherf A, Wahlgren M, (2009). Methods in Malar Res www MR 4org/Portals/3/Methods_In_Malaria_Research-5theditionv5-2 pdf.
49. Dahlbäck 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. doi:10.1186/1475-2875-6-78. PubMed: 17565661.
50. Salanti A, Jensen AT, Zornig HD, Staalsoe T, Joergensen L, et al. (2002) A sub-family of common and highly conserved Plasmodium falciparum var genes. Mol Biochem Parasitol 122: 111-115. doi:10.1016/S0166-6851(02)00080-4. PubMed: 12076777.
51. 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. doi:10.1371/journal.pone.0006667. PubMed: 19690615.
52. 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. doi:10.1186/1475-2875-7-108. PubMed: 18549480.
53. Dahlbäck M, Jørgensen LM, Nielsen MA, Clausen TM, Ditlev SB, et al. (2011) The chondroitin sulfate A-binding site of the VAR2CSA protein involves multiple N-terminal domains. J Biol Chem 286: 15908-15917. doi:10.1074/jbc.M110.191510. PubMed: 21398524.
54. Mmbando BP, Vestergaard LS, Kitua AY, Lemnge MM, Theander TG, et al. (2010) A progressive declining in the burden of malaria in north-eastern Tanzania. Malar J 9: 216. doi:10.1186/1475-2875-9-216. PubMed: 20650014.
55. Mmbando BP, Lusingu JP, Vestergaard LS, Lemnge MM, Theander TG, et al. (2009) Parasite threshold associated with clinical malaria in areas of different transmission intensities in north eastern Tanzania. BMC Med Res Methodol 9: 75. doi:10.1186/1471-2288-9-75. PubMed: 19909523.
56. 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. doi:10.1186/1475-2875-7-101. PubMed: 18533996.
57. Joergensen L, Bengtsson DC, Bengtsson A, Ronander E, Berger SS, et al. (2010) Surface co-expression of two different PfEMP1 antigens on single Plasmodium falciparum-infected erythrocytes facilitates binding to ICAM1 and PECAM1. PLOS Pathog 6: e1001083. PubMed: 20824088.
58. Wang CW, Lavstsen T, Bengtsson DC, Magistrado PA, Berger SS, et al. (2012) Evidence for in vitro and in vivo expression of the conserved var3 (type 3) Plasmodium falciparum erythrocyte membrane protein 1. Malar J 11: 129. doi:10.1186/1475-2875-11-129. PubMed: 22533832.
59. Brown A, Turner L, Christoffersen S, Andrews KA, Szestak T, et al. (2013) Molecular architecture of a complex between an adhesion protein from the malaria parasite and intracellular adhesion molecule 1. J Biol Chem 288: 5992-6003. doi:10.1074/jbc.M112.416347. PubMed: 23297413.
60. Albrecht L, Moll K, Blomqvist K, Normark J, Chen Q, et al. (2011) var gene transcription and PfEMP1 expression in the rosetting and cytoadhesive Plasmodium falciparum clone FCR3S1.2. Malar J 10: 17. doi:10.1186/1475-2875-10-17. PubMed: 21266056.
61. Lavstsen T, Turner L, Saguti F, Magistrado P, Rask TS, et al. (2012) Plasmodium falciparum erythrocyte membrane protein 1 domain cassettes 8 and 13 are associated with severe malaria in children. Proc Natl Acad Sci U S A 109: E1791-E1800. doi:10.1073/pnas.1120455109. PubMed: 22619319.
62. Hviid L, (2011) The case for PfEMP1-based vaccines to protect pregnant women against Plasmodium falciparum malaria. Expert Rev Vaccines 10: 1405-1414. doi:10.1586/erv.11.113. PubMed: 21988306.
63. Hviid L, (2005) Naturally acquired immunity to Plasmodium falciparum malaria in Africa. Acta Trop 95: 270-275. doi:10.1016/j.actatropica.2005.06.012. PubMed: 16018958.
64. 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. PubMed: 17182581.
65. Bengtsson A, Joergensen L, Rask TS, Olsen RW, Andersen MA, et al. (2013) A novel domain cassette identifies Plasmodium falciparum PfEMP1 proteins binding ICAM-1 and is a target of cross-reactive, adhesion-inhibitory antibodies. J Immunol 190: 240-249. doi:10.4049/jimmunol.1202578. PubMed: 23209327.
66. Barfod L, Nielsen MA, Turner L, Dahlbäck 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. doi:10.1128/IAI.01617-05. PubMed: 16790811.
67. Nielsen MA, Pinto VV, Resende M, Dahlbäck M, Ditlev SB, et al. (2009) Induction of adhesion-inhibitory antibodies against placental Plasmodium falciparum parasites by using single domains of VAR2CSA. Infect Immun 77: 2482-2487. doi:10.1128/IAI.00159-09. PubMed: 19307213.
68. Vigan-Womas I, Guillotte M, Juillerat A, Hessel A, Raynal B, et al. (2012) Structural basis for the ABO blood-group dependence of Plasmodium falciparum rosetting. PLOS Pathog 8: e1002781. PubMed: 22807674.
69. Bigey P, Gnidehou S, Doritchamou J, Quiviger M, Viwami F, et al. (2011) The NTS-DBL2X region of VAR2CSA induces cross-reactive antibodies that inhibit adhesion of several Plasmodium falciparum isolates to chondroitin sulfate A. J Infect Dis 204: 1125-1133. doi:10.1093/infdis/jir499. PubMed: 21881129.
70. Barfod L, Dobrilovic T, Magistrado P, Khunrae P, Viwami F, et al. (2010) Chondroitin sulfate A-adhering Plasmodium falciparum-infected erythrocytes express functionally important antibody epitopes shared by multiple variants. J Immunol 185: 7553-7561. doi:10.4049/jimmunol.1002390. PubMed: 21078904.
71. Ghumra A, Semblat JP, Ataide R, Kifude C, Adams Y, et al. (2012) Induction of strain-transcending antibodies against Group A PfEMP1 surface antigens from virulent malaria parasites. PLOS Pathog 8: e1002665.
72. Salanti A, Resende M, Ditlev SB, Pinto VV, Dahlbäck M, et al. (2010) Several domains from VAR2CSA can induce Plasmodium falciparum adhesion-blocking antibodies. Malar J 9: 11. doi:10.1186/1475-2875-9-S2-O11. PubMed: 20064234.
73. 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. doi:10.1084/jem.192.1.1. PubMed: 10880521.
74. Heddini A, Chen Q, Obiero J, Kai O, Fernandez V, et al. (2001) Binding of Plasmodium falciparum-infected erythrocytes to soluble platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): frequent recognition by clinical isolates. Am J Trop Med Hyg 65: 47-51. PubMed: 11504407.